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J Comp Neurol. 2016 Aug 15;524(12):2440-61. doi: 10.1002/cne.23961. Epub 2016 Feb 8.

Development of early-born γ-Aminobutyric acid hub neurons in mouse hippocampus from embryogenesis to adulthood.

Villette V1,2,3, Guigue P1,2,3, Picardo MA1,2,3, Sousa VH1,2,3, Leprince E1,2,3, Lachamp P1,2,3, Malvache A1,2,3, Tressard T1,2,3, Cossart R1,2,3, Baude A1,2,3.

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INSERM U901, Marseille, 13009, France.
Aix-Marseille University, UMR 901, Marseille, 13009, France.
INMED, Marseille, 13009, France.


Early-born γ-aminobutyric acid (GABA) neurons (EBGNs) are major components of the hippocampal circuit because at early postnatal stages they form a subpopulation of "hub cells" transiently supporting CA3 network synchronization (Picardo et al. [2011] Neuron 71:695-709). It is therefore essential to determine when these cells acquire the remarkable morphofunctional attributes supporting their network function and whether they develop into a specific subtype of interneuron into adulthood. Inducible genetic fate mapping conveniently allows for the labeling of EBGNs throughout their life. EBGNs were first analyzed during the perinatal week. We observed that EBGNs acquired mature characteristics at the time when the first synapse-driven synchronous activities appeared in the form of giant depolarizing potentials. The fate of EBGNs was next analyzed in the adult hippocampus by using anatomical characterization. Adult EBGNs included a significant proportion of cells projecting selectively to the septum; in turn, EBGNs were targeted by septal and entorhinal inputs. In addition, most EBGNs were strongly targeted by cholinergic and monoaminergic terminals, suggesting significant subcortical innervation. Finally, we found that some EBGNs located in the septum or the entorhinal cortex also displayed a long-range projection that we traced to the hippocampus. Therefore, this study shows that the maturation of the morphophysiological properties of EBGNs mirrors the evolution of early network dynamics, suggesting that both phenomena may be causally linked. We propose that a subpopulation of EBGNs forms into adulthood a scaffold of GABAergic projection neurons linking the hippocampus to distant structures. J. Comp. Neurol. 524:2440-2461, 2016.


AB_10000240; AB_10550535; AB_2270299; AB_2302603; AB_2531897; AB_477329; AB_887864; inducible genetic fate mapping; long-range projecting GABA neuron; nif-0000-10294; operational hub

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